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INVITED REVIEW American Clinical Neurophysiology Society Standardized EEG Terminology and Categorization for the Description of Continuous EEG Monitoring in Neonates: Report of the American Clinical Neurophysiology Society Critical Care Monitoring Committee Tammy N. Tsuchida,* Courtney J. Wusthoff,Renée A. Shellhaas,Nicholas S. Abend,§k Cecil D. Hahn,¶ Joseph E. Sullivan,# Sylvie Nguyen,** Steven Weinstein,* Mark S. Scher,†† James J. Riviello,‡‡ and Robert R. Clancy§k (J Clin Neurophysiol 2013;30: 161173) BACKGROUND Critically ill neonates are at high risk for adverse neurologic sequelae, but the bedside evaluation of a neonates neurologic status, especially cortical functioning, is extremely limited. In such circum- stances, continuous video EEG provides particularly useful informa- tion about brain function and can identify electroencephalographic seizures without clinical correlate (Clancy et al., 1988; Murray et al., 2008). For these reasons, continuous video EEG monitoring is a use- ful tool in the intensive care nursery. The American Clinical Neuro- physiology Society has recently produced guidelines regarding methods and indications for continuous EEG monitoring in neonates (Shellhaas et al., 2011). A challenge in EEG monitoring of neonates is to understand the clinical signicance of various EEG patterns. In the adult population in intensive care unit, there has been extensive debate, for example, regarding the importance of uctuating rhythmic patterns (Hirsch et al., 2004; Oddo et al., 2009; Orta et al., 2009; Vespa et al., 1999). The American Clinical Neurophysiology Society Critical Care Monitoring Committee has generated standardized terminology of rhythmic EEG patterns in the critically ill to facilitate multicenter collaborations to determine whether these patterns have clinical signicance (Hirsch et al., 2005). Neonates have distinctive EEG patterns that necessitate separate terminology. This document is the consensus of experts to establish stan- dardized neonatal EEG nomenclature aimed at improving consistency and facilitating collaborative research. Where evidence exists to support a particular denition, it is noted. For terms with historically variable denitions, alternative nomenclature is referenced but a single denition is proposed. We anticipate that future revisions will incorporate feedback and emerging research building on this initial effort. Many of the studies on which these criteria are based used routine-length EEG recordings, and in this limited context, values such as acceptable duration of interburst intervals have been offered. However, greater variability may be expected in recordings of longer duration. It is hoped that this document provides groundwork for collaboration to determine the clinical signicance of various EEG patterns in continuous monitoring of the critically ill neonate. DETAILS TO BE REPORTED Characterization of a 24-hour period of continuous video EEG recording should include the following (Table 1). 1. Documentation of the patients postmenstrual age (PMA ¼ gestational age, measured from the time of the last men- strual period 1 chronological age) at the time of recording (Engle, 2004) (We use the term PMA in accordance with the American Academy of Pediatrics policy statement on age terminology in the perinatal period. However, we rec- ognize that historically, many seminal investigations of EEG ontogeny calculated gestational age from the time of conception rather than the last menstrual period. This has been traditionally termed conceptional age (CA). The LMP occurs approximately 2 weeks before conception.). a) Term ¼ 37 up to 44 weeks of PMA b) Preterm ¼ less than 37 weeks of PMA c) Post term ¼ 44 to 48 weeks of PMA 2. Documentation of neuroactive medications at the time of recording. This includes sedatives, hypnotics, anxiolytics, general anesthesia, and antiepileptic drugs. An ideal report would also document when these medications are admin- istered during the recording. From the *Department of Neurology and Pediatrics, Childrens National Medical Center, George Washington University School of Medicine; Department of Child Neurology, Stanford University School of Medicine, Lucile Packard Childrens Hospital; Department of Pediatrics and Communicable Diseases, University of Michigan, Ann Arbor, Michigan, U.S.A.; Departments of §Neu- rology and kPediatrics, The Childrens Hospital of Philadelphia, The University of Pennsylvania School of Medicine; ¶Division of Neurology, Department of Paediatrics, The Hospital for Sick Children Research Institute, The Hospital for Sick Children, University of Toronto; #Department of Neurology and Pediatrics, UC San Francisco Pediatric Epilepsy Center, University of California San Francisco; **Child Neurology Unit, Laboratoire Ingenierie Systeme Automatises EA4094, LUNAM University Hospital Angers; ††Pediatric Neurointensive Care Program/Fetal Neurology Program Rainbow Babies, Rainbow Neurological Center, Neurological Institute of University Hospitals, and Childrens Hospital University Hospitals Case Medical Center; and ‡‡NYU Comprehensive Epi- lepsy Center, NYU Langone Medical Center, Division of Pediatric Neurology, Department of Neurology, New York University School of Medicine. Tammy N. Tsuchida and Courtney J. Wusthoff have contributed equally to this manuscript. Address correspondence and reprint requests to Nicholas S. Abend, MD, CHOP Neurology, Wood 6, 34th Street and Civic Center Boulevard, Philadelphia, PA 19104, U.S.A.; e-mail: [email protected]. Copyright Ó 2013 by the American Clinical Neurophysiology Society ISSN: 0736-0258/13/3002-0161 Journal of Clinical Neurophysiology Volume 30, Number 2, April 2013 161

Transcript of American Clinical Neurophysiology Society Standardized EEG … · 2015. 2. 9. · 50 mV...

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INVITED REVIEW

American Clinical Neurophysiology Society Standardized EEGTerminology and Categorization for the Description of

Continuous EEG Monitoring in Neonates:Report of the American Clinical Neurophysiology Society Critical

Care Monitoring Committee

Tammy N. Tsuchida,* Courtney J. Wusthoff,† Renée A. Shellhaas,‡ Nicholas S. Abend,§k Cecil D. Hahn,¶Joseph E. Sullivan,# Sylvie Nguyen,** Steven Weinstein,* Mark S. Scher,†† James J. Riviello,‡‡

and Robert R. Clancy§k

(J Clin Neurophysiol 2013;30: 161–173)

BACKGROUNDCritically ill neonates are at high risk for adverse neurologic

sequelae, but the bedside evaluation of a neonate’s neurologic status,especially cortical functioning, is extremely limited. In such circum-stances, continuous video EEG provides particularly useful informa-tion about brain function and can identify electroencephalographicseizures without clinical correlate (Clancy et al., 1988; Murray et al.,2008). For these reasons, continuous video EEG monitoring is a use-ful tool in the intensive care nursery. The American Clinical Neuro-physiology Society has recently produced guidelines regardingmethods and indications for continuous EEG monitoring in neonates(Shellhaas et al., 2011).

A challenge in EEG monitoring of neonates is to understandthe clinical significance of various EEG patterns. In the adult populationin intensive care unit, there has been extensive debate, for example,regarding the importance of fluctuating rhythmic patterns (Hirsch et al.,2004; Oddo et al., 2009; Orta et al., 2009; Vespa et al., 1999). TheAmerican Clinical Neurophysiology Society Critical Care MonitoringCommittee has generated standardized terminology of rhythmic EEG

patterns in the critically ill to facilitate multicenter collaborations todetermine whether these patterns have clinical significance (Hirschet al., 2005). Neonates have distinctive EEG patterns that necessitateseparate terminology.

This document is the consensus of experts to establish stan-dardized neonatal EEG nomenclature aimed at improving consistencyand facilitating collaborative research. Where evidence exists tosupport a particular definition, it is noted. For terms with historicallyvariable definitions, alternative nomenclature is referenced but a singledefinition is proposed. We anticipate that future revisions willincorporate feedback and emerging research building on this initialeffort. Many of the studies on which these criteria are based usedroutine-length EEG recordings, and in this limited context, values suchas acceptable duration of interburst intervals have been offered.However, greater variability may be expected in recordings of longerduration. It is hoped that this document provides groundwork forcollaboration to determine the clinical significance of various EEGpatterns in continuous monitoring of the critically ill neonate.

DETAILS TO BE REPORTEDCharacterization of a 24-hour period of continuous video EEG

recording should include the following (Table 1).

1. Documentation of the patient’s postmenstrual age (PMA ¼gestational age, measured from the time of the last men-strual period 1 chronological age) at the time of recording(Engle, 2004) (We use the term PMA in accordance withthe American Academy of Pediatrics policy statement onage terminology in the perinatal period. However, we rec-ognize that historically, many seminal investigations ofEEG ontogeny calculated gestational age from the timeof conception rather than the last menstrual period. Thishas been traditionally termed conceptional age (CA). TheLMP occurs approximately 2 weeks before conception.).

a) Term ¼ 37 up to 44 weeks of PMAb) Preterm ¼ less than 37 weeks of PMAc) Post term ¼ 44 to 48 weeks of PMA

2. Documentation of neuroactive medications at the time ofrecording. This includes sedatives, hypnotics, anxiolytics,general anesthesia, and antiepileptic drugs. An ideal reportwould also document when these medications are admin-istered during the recording.

From the *Department of Neurology and Pediatrics, Children’s National MedicalCenter, George Washington University School of Medicine; †Department ofChild Neurology, Stanford University School of Medicine, Lucile PackardChildren’s Hospital; ‡Department of Pediatrics and Communicable Diseases,University of Michigan, Ann Arbor, Michigan, U.S.A.; Departments of §Neu-rology and kPediatrics, The Children’s Hospital of Philadelphia, The Universityof Pennsylvania School of Medicine; ¶Division of Neurology, Department ofPaediatrics, The Hospital for Sick Children Research Institute, The Hospital forSick Children, University of Toronto; #Department of Neurology and Pediatrics,UC San Francisco Pediatric Epilepsy Center, University of California SanFrancisco; **Child Neurology Unit, Laboratoire Ingenierie Systeme AutomatisesEA4094, LUNAM University Hospital Angers; ††Pediatric Neurointensive CareProgram/Fetal Neurology Program Rainbow Babies, Rainbow NeurologicalCenter, Neurological Institute of University Hospitals, and Children’s HospitalUniversity Hospitals Case Medical Center; and ‡‡NYU Comprehensive Epi-lepsy Center, NYU Langone Medical Center, Division of Pediatric Neurology,Department of Neurology, New York University School of Medicine.

Tammy N. Tsuchida and Courtney J. Wusthoff have contributed equally to thismanuscript.

Address correspondence and reprint requests to Nicholas S. Abend, MD, CHOPNeurology, Wood 6, 34th Street and Civic Center Boulevard, Philadelphia, PA19104, U.S.A.; e-mail: [email protected].

Copyright � 2013 by the American Clinical Neurophysiology SocietyISSN: 0736-0258/13/3002-0161

Journal of Clinical Neurophysiology � Volume 30, Number 2, April 2013 161

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3. Documentation of the depth and duration of hypothermiaduring the recording, and whether it is spontaneous orinduced.

4. An ideal report would also document the clinical changesthat have the potential to impact cerebral function. Thesewould include sudden hemodynamic instability, rapidchanges in respiratory function, or cardiorespiratory failure.

5. Documentation of the number of hours of recording thatcannot be interpreted as a result of technical problems.

6. Detailed characterization of the background EEG featuresduring the first hour of recording. Presence or absence ofstate changes must be included.

7. Characterization of 1 hour of background recording withineach 24-hour period of EEG monitoring.

8. Characterization of additional epochs of background whenthere are relevant changes. Relevant changes include evi-dence for not only the increasing encephalopathy but alsothe new development of episodic state changes.

9. Documentation of seizure onset, seizure burden, and sei-zure resolution. When present, specific note should also bemade of the beginning and end of status epilepticus.

The normal neonatal EEG evolves as the brain matures,reflecting both antenatal and postnatal experiences. All else beingequal, two healthy infants with the same PMA should have verysimilar appearing EEG recordings. There should be no visibledifferences between an EEG recorded from a 5-week chronologicalage infant born at 35 weeks of estimated gestational age (PMA ¼ 40weeks) compared with a 1-week chronological age baby born at 39weeks EGA (PMA is also 40 weeks). However, in contrast to the olderchild or adult, the age difference of a few weeks can cause visiblechanges in normal EEG features. The following text proposes nomen-clature to describe normal and abnormal features of the EEG in thepreterm and term infants. Where relevant, it refers to the specific PMAat which various features are seen. We focus specifically on normalstate changes, background features, graphoelements (or named neo-natal EEG features), seizures, and rhythmic or periodic patterns.

BEHAVIORAL STATEStandardized descriptions of the behavioral state and sleep–

wake cycling are particularly useful in considering whether a neo-natal record is normal or abnormal. Features of a full-term neonatalEEG and polysomnographic recording emerge over time in the pre-mature infant. A behavioral state is said to be present when featuresof that state are present for 1 minute or longer (Table 2).

Awake

TermA healthy term neonate is awake when the eyes are open, and

the EEG background has continuous, low to medium voltage [25–50 mV peak-to-peak (pp)] mixed frequency activity with a predom-inance of theta and delta and overriding beta activity (Fig. 1) (allvoltages included in this article refer to pp values). This is tradition-ally called activité moyenne, roughly meaning “average or medium”

EEG background activity. During wakefulness, term infants haveirregular respirations, and there are spontaneous movements of thelimbs and body.

PretermA healthy preterm infant is considered awake when the eyes

are open. This remains its premier clinical characteristic until 32 to34 weeks of PMA, when other polysomnographic signs (irregularrespiratory patterns, phasic or tonic chin EMG activity, and thepresence of small and large body movements) are also reliablyconcordant with wakefulness. Brief portions of the awake EEG arecontinuous at 28 weeks of PMA. The awake background is evenmore continuous by 32 weeks and persistently continuous by 34weeks and thereafter.

SleepSleep in the neonate is classified as active, quiet, transitional,

and indeterminate. Each has distinctive EEG and polysomnographicfeatures.

Active SleepTerm. The healthy term neonate in active sleep has the eyes

closed, intermittent periods of rapid eye movements, and irregularrespirations with small and large body movements. The EEGbackground shows activité moyenne, indistinguishable from that ofnormal wakefulness.

Preterm. Tracé discontinu describes the normal discontinuoustracing encountered in healthy preterm babies (Figs. 1, 2A). This EEGpattern is characterized by bursts of high voltage (50–300 mV pp)activity that are regularly interrupted by low voltage interburst periods(,25 mV pp) (Clancy and Wusthoff, 2011). The duration of the lowvoltage interburst periods is dependent on PMA, being longest in theyoungest PMA infants. The bursts of EEG activity have expected andrecognizable constituents such as monorhythmic occipital delta activ-ity and other patterns that are described below. Tracé discontinu pre-dominates before 28 weeks of PMA. Brief and inconsistent periods ofcontinuous EEG activity occur first in waking state and active sleepalong with rapid eye movements at 25 weeks of PMA (Scher et al.,2005a). Movements (face and body) in active sleep tend to be seg-mental myoclonus or generalized myoclonic and tonic posturing. By28 to 31 weeks of PMA, there are some periods with complete

TABLE 1. Details to Include in Daily EEG Report

Patient PMANeuroactive medications in use during recordingUse of hypothermia during recordingClinical changes that may impact cerebral functionDocumentation of duration of recording (in hours)

uninterpretable as a result of technical problemsCharacterization of background features during first hour of monitoringCharacterization of 1 hour of background within each

subsequent 24-hour epochCharacterization of additional epochs when background changesSeizure onset, burden, and resolutionPresence, onset, and resolution of status epilepticus

TABLE 2. Behavioral State

AwakeAsleepActive SleepQuiet Sleep

Transitional SleepIndeterminate SleepSleep–wake cycling

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features of active sleep (eyes closed, rapid eye movements, irregularrespirations, body movements, and continuous EEG). After 34 weeks,active sleep consistently has continuous EEG activity.

Quiet SleepTerm. In the healthy term neonate, quiet sleep is clinically

characterized by eye closure, absence of rapid eye movements, andscant body movements, except for occasional sucking activity orgeneralized myoclonic “startles.” The quiet sleep EEG backgroundnear term, tracé alternant, evolves from the less mature tracé discon-tinu in the preterm (Figs. 1, 2B). It shows the “alternating tracing” inwhich higher voltage bursts (50–150 mV pp), comprised predomi-nantly of delta activity and lasting roughly 4 to 10 seconds, alternatewith briefer, lower voltage (25–50 mV pp) (Lamblin et al., 1999)interburst periods composed mostly of mixed theta and delta activity.These interburst periods of tracé alternant, taken in isolation, greatlyresemble the characteristics of activité moyenne with its low tomedium voltage, mixed frequency activity. Tracé alternant graduallydisappears with age and is minimal by 42 weeks and vanishes by46 weeks. As tracé alternant fades, it is replaced in quiet sleep by themore mature, fully continuous quiet sleep background composed ofnonstop, high-voltage (50–150 mV pp) delta and theta activity. Sleepspindles around 10 to 12 Hz first appear within this continuous slowwave sleep pattern by 46 weeks of PMA.

Preterm. In the very preterm neonate, most of the EEGbackground is discontinuous in all behavioral states. With advancingPMA, wakefulness and active sleep are distinguished from quietsleep by greater periods of continuity. Tracé discontinu is the defin-ing feature of quiet sleep first emerging approximately 28 weeks ofPMA. By 34 to 36 weeks, tracé discontinu is seen only in quiet sleep.The amount of time with a tracé discontinu pattern decreases withincreasing PMA so that a term infant has rare, if any, periods of tracédiscontinu in quiet sleep (Hahn et al., 1989). By 37 to 40 weeks,tracé alternant fully replaces tracé discontinu, as described above.

Transitional SleepIn between states of waking, active sleep, and quiet sleep,

there are temporary transitional periods in which typical features fora specific behavioral state are incomplete. These transitional sleepstates typically blend together clinical and EEG features of the orig-inal and final behavioral states. Transitional sleep does not clearlysatisfy the polysomnographic and EEG background criteria for a spe-cific state, as defined above. For example, in the transition fromactive sleep to quiet sleep, an infant might still show some largebody movement but deep regular respirations accompanied by anEEG that is between activité moyenne and tracé alternant. Thisadmixture of the two states is seen until quiet sleep fully emergesand satisfies all the criteria for definite quiet sleep. Transitional sleepcan be thought of as a temporary period of indeterminate sleep, asdescribed below.

Indeterminate SleepSegments of the EEG in which the baby’s eyes are closed

(indicating sleep) but in which other clinical and EEG features donot permit definite assignment to active or quiet sleep are designatedas indeterminate sleep. These periods lack the anticipated features forassignment to a unique sleep state. As above, transitional sleep is atemporary kind of indeterminate sleep. Much of the sleep is indeter-minate in very preterm infants in whom there is not a well-establishedconcordance between the EEG background and polysomnographicvariables. Only a small amount of total sleep time is indeterminatein healthy term infants. A high percentage of total sleep time that isindeterminate would be considered abnormal at term.

Sleep–Wake CyclingSleep–wake cycling is the pattern of alterations among behav-

ioral states. Cycling is more distinctive and easier to recognize interm babies, compared with preterm babies. It is also easier to detectin long-term recordings than brief routine tracings (Scher et al.,2005a).

FIG. 1. Examples of EEG backgroundclassification by voltage.

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Term. In the term infant, a complete sleep and waking cycletypically has a duration of 3 to 4 hours (Scher et al., 2005b). Anisolated sleep-only cycle typically lasts 40 to 70 minutes andprogresses in a somewhat orderly fashion. The awake term infantusually first falls into an active sleep state. This is true until about4 months after term equivalent age. Tracé alternant may thenappear in the first portion of quiet sleep and gradually be replacedby continuous high-voltage slow activity. Term neonates spendapproximately 50% to 60% of the sleep cycle in activesleep, 30% to 40% in quiet sleep, and 10% to 15% in transitionalsleep.

Preterm. The proportion of time spent in any state also variesby age (Curzi-Dascalova et al., 1988; Scher et al., 2005a). The firstrudimentary evidence of sleep cycling can be seen at 25 weeks ofPMA. At 27 to 34 weeks of PMA, 40% to 45% is spent in activesleep, 25% to 30% in quiet sleep, and 30% in indeterminate sleep.Beyond 35 weeks of PMA, infants spend 55% to 65% of the time inactive sleep, 20% in quiet sleep, and 10% to 15% in indeterminatesleep. The duration of a sleep cycle (first active sleep, then transi-tional sleep and finally quiet sleep) is 30 to 50 minutes for neonates,35 weeks of PMA and increases to 50 to 65 minutes beyond 35weeks of PMA.

Unspecified state changes. In a sick infant with disruption ofnormal background features, it may be difficult or impossible toidentify definite specific sleep states. However, some infants can stillhave state changes, defined as cycling between distinctly differentEEG patterns as indicated by the amount of background

discontinuity, voltages, or electrical frequencies with at least 1 minutein each unspecified state.

EEG BACKGROUNDThe constituents of normal neonatal EEG background evolve

with PMA. In the following section, the features of both normal andabnormal EEG backgrounds will be defined (Table 3).

FIG. 2. Examples illustrating the contrasts between trace discontinu, trace alternant, excessive discontinuity, and burstsuppression. EEG tracings courtesy of Clancy and Wusthoff, 2011. A, In trace discontinu, the bursts are separated by very lowvoltage, suppressed IBIs. There are no artifacts from EMG activity or movement, and the respiratory pattern is quite regular. B, Inthis example of trace alternant, however, there is an alternating pattern of high and low voltages but no periods that areconsistently suppressed. There are no artifacts from EMG activity or movement, and the respiratory pattern is quite regular. C, Thisexcessively discontinuous record from a term infant with an acute encephalopathy showing prolonged IBIs, although with somenormal features present during bursts, such as the conspicuous encoche frontale seen near its onset (arrow). D, Burst suppression,in contrast, contains prolonged, extremely suppressed IBIs and bursts composed exclusively of abnormal electrical activity.

TABLE 3. EEG Background

ContinuityNormal continuityNormal discontinuityExcessive discontinuityBurst suppression

SymmetrySynchronyVoltageNormal voltageBorderline low voltageAbnormally low voltageLow voltage suppressedElectrocerebral inactivity

VariabilityReactivityDysmaturity

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Continuity

Normal ContinuityEEG activity is continuous when there is uninterrupted,

nonstop electrical activity with ,2 seconds of voltage attenuation,25 mV pp. The entire evolution of the normal EEG backgroundproceeds from the persistently discontinuous tracing in all behavioralstates in extremely premature infants to continuous EEG in all statesin fully mature infants.

DiscontinuityDiscontinuous EEG activity is broadly recognized as higher

voltage “bursts” of electrical activity interrupted by lower voltage“interbursts.” The intervening periods of attenuation are termedinterburst intervals (IBI). The durations in seconds of the IBIs area function of age, being longest in very preterm infants and shortestduring tracé alternant quiet sleep at term. We define the IBI as aperiod in which activity is attenuated,25 to 50 mV pp for 2 secondsor more. The literature has historically proposed various definitionsfor classifying EEG patterns on the basis of IBI. The definitionsoffered here are attempted compromises from these (Hahn et al.,1989; Lamblin et al., 1999) (Table 4). The background can still becalled discontinuous if there is modest activity within the IBI ina single electrode or a single transient in multiple electrodes.

Normal DiscontinuityThere is a progressive decrease in normal IBI durations with

increasing PMA (Hahn et al., 1989; Lamblin et al., 1999). Tracédiscontinu, as defined above, is a normal discontinuous EEG patternin preterm infants (Figs. 1, 2A). The electrical activity within thebursts includes age-appropriate graphoelements such as rhythmicoccipital delta activity and other specific, named patterns that aredescribed below. It is present in varying amounts from 26 to 40weeks of PMA. It appears first in wakefulness, active and quiet sleep(until 30 weeks of PMA), then only in quiet sleep and is rarely seenin infants of 38-week PMA or older (Hahn et al., 1989).

Tracé alternant, as already defined, depicts a point of transi-tion from complete discontinuity to full continuity. It is only seen inquiet sleep. In the transition from tracé discontinu to tracé alternant,the durations of the IBIs shorten while their voltages swell until allthe gaps of immature discontinuity have been filled in. While burstsof 50 to 150 mV delta activity alternate with lower voltage thetaactivity of 25 to 50 mV, these lower voltage periods never com-pletely attenuate. In contrast to tracé discontinu, the voltages arenever ,25 mV pp (Lamblin et al., 1999) (Figs. 1, 2B). Like tracédiscontinu, the abundance of this pattern varies by age. Tracé alter-nant is first seen at 34 to 36 weeks of PMA, which becomes minimalby 42 weeks and is no longer seen by 46 weeks of PMA.

Excessive Background DiscontinuityIn sick newborn infants who have experienced a variety of

causes of encephalopathy (such as HIE, intracerebral bleeding, septicmeningitis, etc.), the two main reported categories of backgroundabnormalities are pathologically excessive discontinuity and abnor-mally low voltage for PMA (Clancy et al., 2011). We suggest restrict-ing the term “excessive discontinuity” to abnormally discontinuoustracings with bursts that contain some normal patterns and graphoele-ments separated by IBIs that are too prolonged or voltage depressed forPMA, as defined by the parameters in Table 4 (Figs. 1, 2C) (Clancyand Wusthoff, 2011). This is an area that can be addressed and betterquantified by future study using standardized methodology to correlateIBI with patient outcomes.

Burst SuppressionFurther disruption of EEG continuity results in the more

severe burst suppression pattern. This consists of invariant, abnor-mally composed EEG bursts separated by prolonged and abnormallylow voltage IBIs periods, strictly defined as IBI voltages ,5 mV pp(Figs. 1, 2D). However, the definition does allow for one electrodewith sparse activity during the IBI up to 15 mV pp or less than 2seconds with transient activity up to 15 mV pp or.2:1 asymmetry involtage in multiple electrodes.

In all cases, the EEG should be invariant, with no spontaneousdiscontinuity changes because of internally mediated lability and noEEG change of reactivity because of external noxious stimulation ofthe infant. The presence of high (.100 mV pp) or low (,100 mV pp)voltage activity in the bursts should be described. The composition ofthe bursts of the EEG activity is characterized by nonspecific theta,delta, beta, and admixed sharp waves but is devoid of specific graph-oelements such as monorhythmic occipital delta activity, deltabrushes, or other recognizable graphoelements. This is a key featuredistinguishing burst suppression from excess discontinuity: burstsuppression has no normal features within the bursts, whereasexcessively discontinuous records have some normal patterns iden-tifiable within the bursts. Similarly, burst suppression is an invariantpattern, whereas excess discontinuity contains some variability orreactivity.

If burst suppression occurs, typical burst and IBI durationshould be recorded. Further characterization should include a descrip-tion of the “sharpness” of the components of a typical burst (seeModifier and Sharpness under Rhythmic and Periodic Patterns ofUncertain Significance). In some individuals, the bursts are com-posed entirely of nonspecific frequencies, but in others, unequivo-cable sharp waves appear admixed within the bursts.

Symmetry

Normal SymmetryIn the normal neonatal EEG, electrical voltages, frequencies,

and the distribution of specific, named graphoelements should bereasonably equally represented between homologous regions of thetwo hemispheres. The left and right hemispheres should be more orless electrographic mirror images of each other. This allows forfleeting, transient asymmetries to occasionally occur, while stillconsidering the record symmetric overall.

Abnormal AsymmetryThe persistence of more than a 2:1 difference in voltages

between homologous regions of the two hemispheres, or a cleardisparity of background features, including the fundamental

TABLE 4. Normal IBI Duration and Amplitude

PMA (Weeks)Maximum InterburstInterval (Seconds)

Voltage ofInterburst (mV)

,30 35 ,2530–33 20 ,2534–36 10 w2537–40 6 .25

Values for IBI duration and amplitude vary with PMA.

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electrical frequencies and the distribution of specific graphoelementsbetween the two sides, is abnormal. Because focal lesions (arterialischemic stroke, sinovenous thrombosis, localized bleeding, abscess,etc.) account for up to 10% of acute neonatal encephalopathies, EEGbackground asymmetries are not rare and may be diagnosticallyrelevant.

SynchronySynchrony is defined as the onset of bursts of activity that

occur nearly simultaneously between hemispheres in the discontin-uous portions of the recording. For example, a single burst withintracé discontinu would be considered synchronous if the onsets ofthe left and right hemisphere bursts occur within 1.5 seconds of eachother. The reader assesses the percentage of bursts that are synchro-nous within the discontinuous portions of the study.

Normal SynchronyThe percentage of synchronized bursts is not a linear function

of PMA. Before 27 to 29 weeks of PMA, EEG activity is almostcompletely synchronous (Clancy et al., 2003; Mizrahi et al., 2004).Between 29 and 30 weeks of PMA, EEG activity may only beapproximately 70% synchronous. From approximately 30 to 37weeks of PMA, more synchronous activity emerges until term whenthe EEG is nearly 100% synchronous again.

Normal AsynchronyAs above, some degree of asynchrony is expected and normal

between 30 and 37 weeks of PMA. By 38 weeks of PMA, the EEGshould not show any substantial amount of asynchrony.

Abnormal AsynchronyThis is defined as a clearly excessive percentage of EEG

bursts for PMA that occur asynchronously (greater than 1.5 secondsbetween the onset of activity in each hemisphere) during thediscontinuous portions of the recording.

VoltageFew studies have defined the normal boundaries for voltage

(or amplitude) in premature infants. Thus, there will be no attempt tooffer normal voltage criteria for abnormality in this group. The focusof this section will therefore be the boundaries of normal voltage forthe term infant (Fig. 1). Just as with the older child or adult, voltageabnormalities should be interpreted with caution because manyextracerebral conditions (such as poor electrode impedance or inac-curate electrode placement, scalp edema, cephalohematoma, andsubdural hemorrhages) can artificially result in low voltage EEGactivity or interhemispheric voltage asymmetries. Strict voltagethresholds are therefore difficult to determine.

Normal VoltageA healthy term infant should have most EEG activity$25 mV pp

in all behavioral states.

Borderline Low VoltageThis is defined as a continuous EEG background containing

some normal activity and graphoelements with representativevoltages persistently at least 10 mV but ,25 mV. The clinical sig-nificance of borderline low voltage is not certain.

Abnormally Low VoltageLow voltage suppressed. There are various definitions in the

literature of an abnormal background because of a low voltage or“low voltage undifferentiated” pattern (Holmes et al., 1982; Monodet al., 1972; Tharp et al., 1981). We propose a definition of persis-tently low voltage activity without normal background features. Thefundamental baseline voltage is ,10 mV pp. The background can beinterspersed with higher voltage ($10 mV pp) transient activity for,2 seconds. In addition, the record is invariant, with no inherentlability, and unreactive, with no EEG changes from external stimu-lation. This pattern suggests severe neurologic injury with diffusedeath or dysfunction of the cortical neuronal generators of EEGactivity.

Electrocerebral inactivity. This terminology is used to describethe absence of discernible cerebral electrical activity $2 mV pp whenreviewed at a sensitivity of 2 mV/mm (Holmes and Lombroso, 1993).The term electrocerebral inactivity (ECI) has largely replaced the pre-vious terms “electrocerebral silence” and isoelectric recordings,although their implications are the same. Published guidelines detailthe technical requirements needed for performing an EEG to assess forECI (American Clinical Neurophysiology Society, 2006). These aredistinct from the technical requirements for standard neonatal EEGrecordings. If the EEG is not performed according to these standards,the term ECI should not be applied. If there is no discernible cerebralactivity, but the recording was not conducted according to the ECIguidelines, the report should indicate that the recording may be con-sistent with ECI but should specify that ECI cannot be determinedwithout the appropriate technical parameters. Electrocerebral inactivityis a pattern which, when coupled with appropriate clinical examinationand/or neuroimaging, is used to determine cerebral death (Ashwal,1989; Ashwal and Schneider, 1989; Holmes and Lombroso, 1993;Nakagawa et al., 2011; Volpe, 1987). Clinicians are advised to consulttheir institutions’ guidelines regarding the determination of brain deathfor newborn infants, as practices vary.

VariabilityVariability (lability) denotes conspicuous spontaneous EEG

responses to internal stimuli such as that occur during typical sleep–wake cycling. It is first present by 25 weeks when the EEG initiallydemonstrates nascent changes with biobehavioral state. Variabilityshould be increasingly apparent by 28 weeks of PMA and wellestablished by 30 to 31 weeks of PMA. The EEG responses canconsist of changes in any electrical domain: frequency, continuity,or voltage. It is important to note that arousals from sleep can resultin transient attenuation of EEG voltages, which should not be mis-taken for discontinuity. Variability should be recorded as yes, no, orunclear/unknown/not applicable. For example, variability wouldobviously be present in a 60-minute recording, which captured mul-tiple behavioral states such as wakefulness, transitional, active, andquiet sleep. The last choice might apply, for example, in a 60-minuterecording that captured only an awake state.

ReactivityReactivity of EEG is demonstrated when there is a conspicu-

ous cerebral EEG response to external stimulation. Like lability,these EEG responses also consist of changes in any electricaldomain: frequency, continuity, or voltage. The clinical and behav-ioral components of reactivity can include crying, movement, EMGactivity, and respiratory pattern changes. It is important to note thatafter internal or external stimulation, behavioral responses may

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induce artifacts from movement or EMG activity that may mimicactual changes of the EEG background. Reactivity first appears at30 to 32 weeks of PMA, but it might not been seen with each andevery external stimulation. Reactivity should be recorded as yes, no,or unclear/unknown/not applicable. Strength and/or nature of stimulusshould be noted.

DysmaturityThe traditional scenario in which the term dysmaturity was

coined involved very premature infants with chronic illnesses suchas bronchopulmonary dysplasia. Over time, their EEG backgroundfeatures sometimes failed to mature at the same rate as their PMAprogressed. There was eventually a gap between their actual PMAand their maturity as suggested by the appearance of their EEGbackgrounds. This disparity in maturity between the actual PMAand their “EEG PMA” is termed dysmaturity, defined as an EEGthat would be normal for an infant at least 2 weeks younger than thestated PMA. The persistently dysmature EEG is considered abnor-mal and is associated with an increased risk of abnormal neurologicoutcome (Biagioni et al., 1996a; Holmes and Lombroso, 1993).

NORMAL GRAPHOELEMENTS (DEVELOPMENTALBACKGROUND HALLMARKS)

In neonatal EEG, graphoelements are normal, expected, andspecific; named EEG background patterns that first appear peak andthen fade during particular epochs of neonatal development. Theyare characteristic of specific PMAs. They are a part of the compositionof the normal EEG background and are thus typically symmetric. Notevery known type of specific graphoelement is included below; wehave defined the most commonly seen (Table 5).

Monorythmic Delta ActivityThis pattern occurs between 24 and 34 weeks of PMA and

consists of moderately high voltage (up to 200 mV pp) delta activitywith a relatively stereotyped morphology. It may be predominantlyoccipital, temporal, and/or central but is rarely frontal (Clancy et al.,2003). Is typically synchronous and symmetric and often surfacepositive.

Delta BrushesDelta brushes have been described under many names,

including beta–delta complexes, spindle-delta bursts, spindle-likefast waves, or ripples of prematurity.

These are most prominent between 24 and 36 weeks of PMAand consist of a combination of 0.3 to 1.5 Hz slow waves of 50 to250 mV pp with superimposed fast activity (8–12 or 18–22 Hz)(Lamblin et al., 1999). Their peak expression is between 32 and34 weeks of PMA. They are maximal in active sleep up to 32 weeksand after that are seen in wakefulness and quiet sleep and then are

maximal in quiet sleep between 33 and 37 weeks of PMA (Clancyet al., 2003; Mizrahi et al., 2004). They are occasionally seen in quietsleep up to 40 weeks of PMA.

Rhythmic Temporal ThetaThis graphoelement occurs between 24 and 34 weeks of PMA.

It typically consists of 25 to 120 mV pp theta frequency activity forshort (2 seconds) bursts over the temporal region. It is typically sym-metric and maximal between 29 and 32 weeks of PMA (Clancy et al.,2003; Lamblin et al., 1999; Mizrahi et al., 2004). Morphologicallysimilar activity can be seen at the vertex and occipital regions.

Anterior DysrhythmiaDespite its somewhat misleading name, this is a normal

graphoelement. It first appears at 32 weeks and persists until 44weeks of PMA. It consists of 50 to 100 mV pp delta waves, whichmay occur in isolation or brief runs for a few seconds over the frontalregions (Clancy et al., 2003; Lamblin et al., 1999). It is typicallysynchronous and symmetric.

Encoches FrontalesThis pattern is intimately related to anterior dysrhythmia and

the two are often seen admixed over the frontal regions (Fig. 3A).Encoches frontales occur between 34 and 44 weeks of PMA andconsist of 50 to 100 mV pp broad diphasic transients (0.5–0.75seconds) with a small initial negative deflection and a larger positivedeflection (Clancy and Wusthoff, 2011; Clancy et al., 2003; Lamblinet al., 1999). Overall, they are typically synchronous and symmetric.They are often present in transitional sleep and most abundant in thetransition from active to quiet sleep (Clancy et al., 2003; Mizrahiet al., 2004).

EEG TRANSIENT PATTERNSAs opposed to the fundamental EEG background, which is the

basic ongoing cerebral electrical activity, there are also transientEEG patterns that may intermittently punctuate the background(Table 6).

Sharp Wave TransientsMany healthy neonates have normal, physiologic sharp wave

transients, whereas some sick newborns show abnormal or excessivesharp wave transients that imply pathologic conditions. Thereremains debate regarding the boundaries that separate physiologicfrom pathologic sharp wave transients. Sharp wave transients arecharacterized by their negative or positive polarity, duration,abundance, spatial distribution, and repetitive behavior.

A negative sharp wave transient has an initial and pre-dominant deflection that is surface negative. A positive sharp wavetransient has an initial and predominant deflection that is surfacepositive. Both need to be clearly distinct from the background asseparate transients and not just “sharply contoured background activ-ity.” Sharp wave transients lasting ,100 milliseconds are commonlycalled spikes. Sharp wave transients lasting 100 to 200 millisecondsare commonly called sharp waves. It is notable that the typical neo-natal display of 15 mm/seconds time compresses the appearance ofthe background, and many EEG features will appear more sharplycontoured than if the recording were viewed at the typical adult orpediatric display setting of 30 mm/second.

TABLE 5. Normal Graphoelements

Monorhythmic delta activityDelta brushesRhythmic temporal thetaAnterior dysrhythmiaEncoches frontales

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FIG. 3. Examples illustrating the contrasts between encoches frontales, physiologic sharp waves, and pathologic sharp waves.A, Encoches frontales are present and synchronous in both frontal regions. B, A physiologic sharp wave is seen in the 13th second,in the right midtemporal region (T4). C, Pathologic periodic sharp waves are seen in the left anterior quadrant. These occurfrequently and repetitively in the same location. The first three are highlighted with arrows.

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Quantification of the abundance of sharp wave transients (thenumber of spike or sharp waves per minute at a given location suchas the central or temporal regions) should be undertaken in the mostcontinuous portions of the neonatal EEG: wakefulness or activesleep. In the discontinuous portions of the record, particularly duringtracé alternant, the EEG bursts often have fleeting sharply contouredactivity embedded within the background, rather than truly distinctEEG transients separate from the background. Sharp wave transientscan appear at any electrode location. Sharp wave transients mayoccur as single, solitary events or recur in brief repetitive runs or trains.

Physiologic Negative Sharp WavesPhysiologic negative sharp waves lasting 100 to 200 milli-

seconds are commonly seen in the EEGs of healthy near-term andterm infants (Fig. 3B). They are typically observed against the back-drop of a normal EEG background for PMA. They appear in greatestabundance in the midtemporal, central, and centrotemporal regions.They are rare in the frontal, midline vertex, and occipital regions.They are symmetrically distributed between homologous regions ofthe hemispheres. They are mostly single, solitary transients, but afew may appear in brief trains or runs (Biagioni et al., 1996a).

Abnormal Negative Sharp Wave TransientsThese appear as sharp waves or true spikes (Fig. 3C). They

most commonly arise in the context of an abnormal EEG back-ground for PMA. Although they may also appear in the familiarmidtemporal, central, or centrotemporal locations, they may beheavily concentrated in one region or hemisphere, rather than beingrandomly or evenly distributed spatially. They may also be seen inatypical locations such as the frontal, midline vertex, or occipitalregions. They may be much more abundant compared with physio-logic negative sharp wave transients. Data for neonates who wereassessed developmentally at 1 year or older indicate that negativesharp waves more frequent than 11 per hour for preterm and 13 perhour for term infants are abnormal (Biagioni et al., 1996b; Clancyand Spitzer, 1985; Karbowski and Nencka, 1980; Rowe et al., 1985;Scher et al., 1994a; Statz et al., 1982). Abnormal negative sharpEEG transients are more likely than physiologic negative sharpwaves to recur in brief runs or trains (Clancy, 1989).

Positive Sharp Wave TransientsHistorically, these were first described in the EEGs of preterm

infants who developed significant intraventricular hemorrhages.Positive sharp waves were described in the rolandic regions (positiverolandic sharp waves), represented by electrodes C3 and C4,although it was later recognized that many were actually maximallysituated at the midline vertex (positive vertex sharp waves) with fieldspread to the adjacent rolandic regions (Clancy and Tharp, 1984). Itis now appreciated that positive rolandic sharp waves and positivevertex sharp waves are most closely pathologically associated with

underlying white matter injury including periventricular leukomala-cia (Novotny et al., 1987).

In the term infant, excessive positive sharp waves in themidtemporal regions can signify underlying focal pathologic condi-tion such a localized hemorrhage or white matter injury. However,these are more difficult to judge because rare scattered temporalsharp waves can be occasionally seen in apparently health terminfants. Previous work suggested that up to 3 per hour for pretermand 1.5 per hour for term neonates may be normal (Chung andClancy, 1991; Scher et al., 1994b).

Brief Rhythmic DischargesThis transient EEG pattern consists of evolving rhythmic

patterns of electrical activity that share many characteristics withseizures but are very brief, with a duration of,10 seconds (Nagarajanet al., 2011; Oliveira et al., 2000; Shewmon, 1990). These have pre-viously been alternatively described in the literature as BIRDs (briefictal/interictal rhythmic/repetitive discharges) and BERDs (brief elec-trographic rhythmic discharges). Given that the true significance ofthese discharges is uncertain, the operational term “brief rhythmicdischarges” (BRD) will be used here. They are usually seen in thecontext of an abnormal EEG background and/or confirmed electro-graphic seizures. Also, BRDs are rarely seen in isolation in a normalEEG. At this time, their pathologic significance is not fully under-stood. However, recent studies in adults suggested that clinical behav-ior changes can coexist with epileptiform discharges under 2 secondsin duration (D’Ambrosio et al., 2009). Similarly, a case series dem-onstrated similar mortality and neurologic disability for infants withBRDs as with seizures (Nagarajan et al., 2011). Further study isneeded to better understand the basis and significance of BRD inthe neonate.

SEIZURES AND STATUS EPILEPTICUS

Neonatal SeizuresNeonatal seizures are traditionally classified as clinical only,

electroclinical, or electrographic only seizures. A clinical only seizureconsists of a sudden paroxysm of abnormal clinical changes that donot correlate with a simultaneous EEG seizure. These clinical changesmay include unnatural posturing, obligatory stereotyped movements,sudden arrested behaviors, or autonomic dysfunction (episodic tachy-cardia or hypertension, flushing, pallor or salivation, etc.). An electro-clinical seizure features definite clinical seizure signs simultaneouslycoupled with an EEG seizure (Mizrahi and Kellaway, 1987). An EEGonly seizure refers to the presence of a definite EEG seizure that doesnot provoke any specific outwardly visible clinical signs. For thepurposes of this document, the term “seizure” hereafter refers to elec-trographic seizures, with or without coupled clinical signs of seizure(Table 7).

An electrographic seizure is a sudden, abnormal EEG eventdefined by a repetitive and evolving pattern with a minimum 2 mV ppvoltage and duration of at least 10 seconds. A seizure is always anabnormal pattern and should not be confused with transient back-ground changes, such as those associated with drowsiness or arousalfrom sleep. “Evolving” is defined as an unequivocal evolution infrequency, voltage, morphology, or location. In contrast, brief rhyth-mic repetitive discharges lasting ,10 seconds but with evolutionwould be considered BRDs and not seizures. Likewise, rhythmic,repetitive activity lasting more than 10 seconds but without evolutionwould be considered periodic discharges or rhythmic activity but not

TABLE 6. EEG Transient Patterns

Negative sharp wave transientsPhysiologic negative sharp wavesAbnormal negative sharp waves

Positive sharp transientsBRD

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a seizure (Fig. 3C). While 2 mV pp defines the boundaries of thebeginning and end of each seizure, the voltages predictably increaseas the seizure evolves and can be up to 150 mV pp or more. Unlikeseizures in older children and adults, there is no minimum electricalfrequency required in the definition of seizure. To be classified asseparate seizures, 10 seconds or more must separate two distinctseizure events (Clancy and Legido, 1987; Scher et al., 1993).

Several aspects of a seizure can be quantified. In the olderchild and adult, the American Clinical Neurophysiology Societystandardized research terminology describes the typical, minimum andmaximum frequency (Hz) during a seizure (Hirsch et al., 2005). This isof uncertain significance in the neonate. Seizure location can bedescribed in terms of the focus (site of onset) and maximal spread,represented by the greatest number of electrodes involved. Recommen-ded terminology to describe seizure spread includes the following:

• Diffuse: asynchronous involvement of all electrodes by focal seiz-ures of extensive geographic distribution. This contrasts with chil-dren and adults who can have truly generalized, synchronous, andsymmetric activity.

• Bilateral independent: a seizure with activity occurring simulta-neously in two regions but which begin, evolve, and behave inde-pendently of each other.

• Migrating: seizure moves sequentially from one hemisphere toanother.

• Lateralized: all of the seizure propagates within a single hemi-sphere (left or right hemisphere).

• When a seizure is restricted to a confined region, it can be furtherdescribed as frontal, central, temporal, occipital or vertex, or it canbe described more broadly as anterior quadrant and posteriorquadrant.

• When multiple seizures arise from a single general region, theycan be classified as unifocal onset.

• Multifocal onset seizures originate from at least three independentfoci with at least one in each hemisphere. It is not uncommon forlocalized lesions such as a stroke to precipitate unifocal seizures,while diffuse insults such as meningitis may provoke multifocalonset seizures.

Seizure burden has been quantified in various ways (Clancyand Legido, 1987; McBride et al., 2000; Murray et al., 2008; Pisaniet al., 2008; Shellhaas et al., 2011). We propose quantifying seizureburden for clinical purposes using one of the following definitions:

1. Frequency: the number of seizures per hour or2. Percent of the record with seizures: the total summed dura-

tion of all the seizures divided by the entire duration of anepoch of interest or

3. Temporal–spatial quantification: The most detailed metricof seizure burden that could be used for research purposesincludes the total summed durations of seizures in eachregion of interest, per hour (Scher et al., 1994c). In thiscase, the neonatal montage could be collapsed into fivenonoverlapping regions of interest: Fp3-T3, C3-O1, Fp4-T4, C4-O2, and Fz-Pz (or alternatively Fp3-C3, T3-O1,Fp4-C4, T4-O2, and Fz-Pz). Thus, each single electrodeis counted only once. The total summed seizure durationscan be calculated separately for each of the five regions ofinterest, which provides a temporal–spatial metric of sei-zure burden. Future work is needed to determine the rela-tive utility of these more labor-intensive methods.

Status EpilepticusThe traditional definition of status epilepticus in children and

adults is a single seizure lasting more than 30 minutes or a series ofseizures lasting at least 30 minutes between which baseline brainfunction has not been restored (Shewmon, 1990). These criteria aredifficult to apply to neonates, given the difficulty assessing theirmental status and the high incidence of coexisting acute encephalop-athy. Consequently, other definitions of neonatal status have beenoffered (Scher et al., 1993). In consensus with the current literature,we propose a status epilepticus as present when the summed durationof seizures comprises $ 50% of an arbitrarily defined 1-hour epoch.In other words, if half or more of any given hour of recording showsseizures, then status epilepticus exists for that epoch.

In a population of neonates with recorded electrographicseizures, the percentage of recording time in which seizures aredetected could range from 1% to 100%. It is recognized that ourdefinition of status is a somewhat arbitrary and that there are no datathat specifically justify the choice of 50% over any other percentagevalue as especially meaningful or significant. Alternative researchdefinitions of status could be explored based on the available dataregarding typical durations of electrographic neonatal seizures. In twostudies in neonates, the median EEG seizure length was 1 minute, with75% of seizures lasting #2.5 minutes (Clancy and Legido, 1987;Shellhaas and Clancy, 2007). In these and another study, the rangeof individual seizure duration was 10 seconds to 46 minutes, and themean seizure length was 2 to 4 minutes (Clancy and Legido, 1987;Scher et al., 1993; Shellhaas and Clancy, 2007). In future studies, itwill be useful to characterize different categories of seizure burden andduration of status epilepticus, as they relate to outcomes.

RHYTHMIC AND PERIODIC PATTERNS OFUNCERTAIN SIGNIFICANCE

Some rhythmic patterns do not demonstrate the unequivocalevolution in frequency, morphology, or location characteristic ofseizures. These are targets of active investigation in the older populationin intensive care unit because they are common and their clinicalsignificance is unclear. Pathologic rhythmic and periodic patterns do

TABLE 7. Seizures and Status Epilepticus

SeizuresDuration $10 secondsLocationDiffuse)LateralizedHemispheric: left and right

FocalFrontalCentralTemporalOccipitalVertex

Quadrant- anterior and posteriorBilateral IndependentMultifocalMigrating

Seizure BurdenNumber of seizures per hour orSummed duration of seizures divided by duration of epoch

Status epilepticus: summed duration of seizures totals $50% of a1-hour epoch

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occur in preterm and term neonates but are not common (Scher andBeggarly, 1989). It is unclear whether research terminology that hasbeen developed in adults is applicable to the neonate (Hirsch et al.,2005). We discuss below the patterns from the adult terminology,which have been described previously in neonatal literature (Table 8).

Patterns

PeriodicPeriodic discharges are defined in the adult terminology as

a pattern in which waveforms have a relatively uniform morphologyand duration; there is a quantifiable interval between consecutivewaveforms and the waveforms recur at nearly regular intervals. “Dis-charges” are defined as waveforms with no more than three phases(i.e., crosses the baseline no more than twice or any waveform lasting0.5 seconds or less, regardless of number of phases). In contrast,bursts are defined as waveforms lasting more than 0.5 seconds andhaving at least four phases (i.e., crosses the baseline at least threetimes). “Nearly regular intervals” is defined as having a cycle length(i.e., period) varying by ,50% from one cycle to the next in themajority (.50%) of cycle pairs (Fig. 3C). Periodic discharges arenot common in neonates but can occur with acute destructive pro-cesses such as herpes simplex virus encephalitis, stroke, or globalhypoxia ischemia (Mikati et al., 1990; Sainio et al., 1983; Scher andBeggarly, 1989).

RhythmicRhythmic delta activity is defined in the adult terminology as

the repetition of a waveform with relatively uniform morphology andduration but without an interval between consecutive waveforms. Toqualify as rhythmic, the duration of one cycle (i.e., the period) of therhythmic pattern must vary by ,50% from the duration of the sub-sequent cycle for the majority (.50%) of cycle pairs. Importantly,this EEG pattern may not be abnormal in neonates and is consistentwith some normal neonatal graphoelements: rhythmic occipital deltaactivity and anterior dysrhythmia.

DurationThe periodic or rhythmic pattern must be present for at least

six cycles (e.g., 1/second for 6 seconds or 3/second for 2 seconds).

LocationLocation can be described in terms of the focus (site of onset)

and maximal spread (maximal electrodes involved). Location can belateralized or diffuse. Lateralized includes unilateral focal/regional/hemispheric and bilateral asymmetric activity. In diffuse activity,there is asynchronous involvement of all electrodes. The term diffusecan be applied to bilateral hemispheric involvement even if theactivity has a restricted field (e.g., bifrontal). Patterns may also bebilateral independent or multifocal.

Additional localizing information may include a descriptionof the predominant location. For diffuse, one can specify frontallypredominant, occipitally predominant, midline predominant, or“generalized, not otherwise specified.” Frontally predominant isdefined as having an amplitude in anterior derivations that is at least50% greater than that in posterior derivations on an ipsilateral ear,average, or noncephalic referential recording. Occipitally predomi-nant is defined as having an amplitude in posterior derivations that isat least 50% greater than that in anterior derivations on an ipsilateralear, average, or noncephalic referential recording. Midline predom-inant is defined as having an amplitude in midline derivations that isat least 50% greater than in parasagittal derivations on an average ornoncephalic referential recording. For lateralized, bilateral indepen-dent, or multifocal patterns, one can specify the area(s) most involved(frontal, central, temporal, occipital or vertex or hemispheric if morespecific localization is not possible) and whether the activity is bilat-eral asymmetric or unilateral. If activity is bilateral but asymmetric, themost involved areas (frontal, central, temporal, occipital or vertex orhemispheric) can be specified over both hemispheres.

ModifiersRhythmic patterns can be further described using “modifier”

terms according to the American Clinical Neurophysiology SocietyStandardized Critical Care EEG Terminology 2012. The modifier“evolving” does not apply to neonates because this defines a neonatalseizure. Three other modifiers that differ from the adult terminologyare discussed below.

DurationIf the pattern is not continuous, then the typical duration of

pattern is specified. Duration categories are provided, and the adultterminology also recommends recording the longest continuousduration.

• $1 hour (“very long”)• 5 to 59 minutes (“long”)• 1 to 4.9 minutes (“intermediate duration”)• 10 to 59 seconds (“brief”)• ,10 seconds (“very brief,” distinct from BRDs for lack ofevolution).

In one study, periodic discharge duration in the preterm infantwas less than 1 minute and more than 1 minute in term infants (Scherand Beggarly, 1989). Only 4 of 592 preterm and term infants hadduration $10 minutes. Thus, while we define duration to be consis-tent with terminology used in the intensive care unit for adult EEG,we recognize that very few neonatal EEG patterns will fall into the“long” or “very long” categories.

PolarityIn neonatal recordings, polarity should be determined in the

traditional bipolar montage and should be specified for the

TABLE 8. Rhythmic and Periodic Patterns of UncertainSignificance

PatternPeriodic dischargesRhythmic delta activity

DurationLocation

LateralizedFocalHemispheric: left and rightBilateral asymmetric

DiffuseBilateral independentMultifocal

Modifiers (subset of American Clinical Neurophysiology SocietyStandardized Critical Care EEG Terminology 2012)DurationPolaritySharpness

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predominant phase (phase with the greatest amplitude) only fora typical discharge. Polarity applies only to periodic discharge andthe spike/sharp component of SW, not rhythmic delta activity. Polar-ity is categorized as positive, negative, or unclear.

SharpnessSharpness applies only to periodic discharge and the spike/

sharp component of SW but not to rhythmic delta activity. Sharpnessshould be specified for a typical discharge for both the predominantphase (phase with greatest amplitude) and the sharpest phase ifdifferent. Sharpness categories include the following:

• Spiky waveforms have a duration measured at the EEG baseline,100 milliseconds.

• Sharp waveforms have a duration of 100 to 200 milliseconds.• Sharply contoured theta and delta waveforms have a sharp wavemorphology [steep slope to one side of the wave and/or pointy atinflection point(s)] but are too long in duration to qualify as a sharpwave.

• Blunt waveforms have a smooth or sinusoidal morphology.

CONCLUSIONThis document is a collaborative effort to standardize the

neonatal EEG terminology. We hope this common language fostersmore effective multicenter collaboration to determine the signifi-cance of continuous EEG findings in critically ill neonates. Futurework may build on this framework to establish the utility of theproposed terms and definitions, both in the research and clinicalrealms. This terminology will be revised and updated based on thefeedback and future research.

REFERENCESAmerican Clinical Neurophysiology Society. Guideline 3: Minimum technical

standards for EEG recording in suspected cerebral death. J Clin Neurophysiol2006;23:97–104.

Ashwal S. Brain death in the newborn. Clin Perinatol 1989;16:501–518.Ashwal S, Schneider S. Brain death in the newborn. Pediatrics 1989;84:429–437.Biagioni E, Bartalena L, Biver P, et al. Electroencephalographic dysmaturity in

preterm infants: a prognostic tool in the early postnatal period. Neuropedi-atrics 1996;27:311–316.

Biagioni E, Boldrini A, Bottone U, et al. Prognostic value of abnormal EEGtransients in preterm and full-term neonates. Electroencephalogr Clin Neuro-physiol 1996;99:1–9.

Chung HJ, Clancy RR. Significance of positive temporal sharp waves in the neo-natal electroencephalogram. Electroencephalogr Clin Neurophysiol1991;79:256–263.

Clancy RR. Interictal sharp EEG transients in neonatal seizures. J Child Neurol1989;4:30–38.

Clancy RR, Legido A. The exact ictal and interictal duration of electroencepha-lographic neonatal seizures. Epilepsia 1987;28:537–541.

Clancy RR, Spitzer AR. Cerebral cortical function in infants at risk for suddeninfant death syndrome. Ann Neurol 1985;18:41–47.

Clancy RR, Tharp BR. Positive rolandic sharp waves in the electroencephalo-grams of premature neonates with intraventricular hemorrhage. Electroence-phalogr Clin Neurophysiol 1984;57:395–404.

Clancy RR, Wusthoff CJ. Brain Monitoring: Normal Neonatal EEG [computerprogram]. Ambler, PA: Moberg Multimedia, 2011.

Clancy RR, Legido A, Lewis D. Occult neonatal seizures. Epilepsia1988;29:256–261.

Clancy RA, Bergqvist AGC, Dlugos DJ. Neonatal electroencephalography. In:Ebersole JS, Pedley TA, eds. Current practice of clinical electroencephalog-raphy. 3rd ed. Philadelphia: Lippincott Williams & Wilkins, 2003:106–234.

Clancy RR, Dicker L, Cho S, et al. Agreement between long-term neonatal back-ground classification by conventional and amplitude-integrated EEG. J ClinNeurophysiol 2011;28:1–9.

Curzi-Dascalova L, Peirano P, Morel-Kahn F. Development of sleep states innormal premature and full-term newborns. Dev Psychobiol 1988;21:431–444.

D’Ambrosio R, Hakimian S, Stewart T, et al. Functional definition of seizureprovides new insight into post-traumatic epileptogenesis. Brain 2009;132:2805–2821.

Engle WA. Age terminology during the perinatal period. Pediatrics 2004;114:1362–1364.

Hahn JS, Monyer H, Tharp BR. Interburst interval measurements in the EEGs ofpremature infants with normal neurological outcome. ElectroencephalogrClin Neurophysiol 1989;73:410–418.

Hirsch LJ, Claassen J, Mayer SA, Emerson RG. Stimulus-induced rhythmic, peri-odic, or ictal discharges (SIRPIDs): a common EEG phenomenon in thecritically ill. Epilepsia 2004;45:109–123.

Hirsch LJ, Brenner RP, Drislane FW, et al. The ACNS subcommittee on researchterminology for continuous EEG monitoring: proposed standardized termi-nology for rhythmic and periodic EEG patterns encountered in critically illpatients. J Clin Neurophysiol 2005;22:128–135.

Holmes GL, Lombroso CT. Prognostic value of background patterns in the neo-natal EEG. J Clin Neurophysiol 1993;10:323–352.

Holmes G, Rowe J, Hafford J, et al. Prognostic value of the electroencephalogramin neonatal asphyxia. Electroencephalogr Clin Neurophysiol 1982;53:60–72.

Karbowski K, Nencka A. Right mid-temporal sharp EEG transients in healthynewborns. Electroencephalogr Clin Neurophysiol 1980;48:461–469.

Lamblin MD, Andre M, Challamel MJ, et al. [Electroencephalography of thepremature and term newborn. Maturational aspects and glossary]. NeurophysiolClin 1999;29:123–219.

McBride MC, Laroia N, Guillet R. Electrographic seizures in neonates correlatewith poor neurodevelopmental outcome. Neurology 2000;55:506–513.

Mikati MA, Feraru E, Krishnamoorthy K, Lombroso CT. Neonatal herpes simplexmeningoencephalitis: EEG investigations and clinical correlates. Neurology1990; 40:1433–1437.

Mizrahi EM, Kellaway P. Characterization and classification of neonatal seizures.Neurology 1987;37:1837–1844.

Mizrahi EM, Hrachovy RA, Kellaway P, Stockard-Pope JE. Atlas of neonatalelectroencephalography. 3rd ed. Philadelphia: Lippincott Williams & Wilkins,2004.

Monod N, Pajot N, Guidasci S. The neonatal EEG: statistical studies and prognosticvalue in full-term and pre-term babies. Electroencephalogr Clin Neurophysiol1972;32:529–544.

Murray DM, Boylan GB, Ali I, et al. Defining the gap between electrographicseizure burden, clinical expression and staff recognition of neonatal seizures.Arch Dis Child Fetal Neonatal Ed 2008;93:F187–F191.

Nagarajan L, Palumbo L, Ghosh S. Brief electroencephalography rhythmic dis-charges (BERDs) in the neonate with seizures: their significance and prog-nostic implications. J Child Neurol 2011.

Nakagawa TA, Ashwal S, Mathur M, Mysore M. Clinical Report–Guidelines forthe determination of brain death in infants and children: an Update of the1987 Task Force Recommendations. Pediatrics 2011.

Novotny EJ Jr, Tharp BR, Coen RW, et al. Positive rolandic sharp waves in theEEG of the premature infant. Neurology 1987;37:1481–1486.

Oddo M, Carrera E, Claassen J, et al. Continuous electroencephalography in themedical intensive care unit. Crit Care Med 2009;37:2051–2056.

Oliveira AJ, Nunes ML, Haertel LM, et al. Duration of rhythmic EEG patterns inneonates: new evidence for clinical and prognostic significance of brief rhyth-mic discharges. Clin Neurophysiol 2000;111:1646–1653.

Orta DS, Chiappa KH, Quiroz AZ, et al. Prognostic implications of periodicepileptiform discharges. Arch Neurol 2009;66:985–991.

Pisani F, Copioli C, Di Gioia C, et al. Neonatal seizures: relation of ictal video-electroencephalography (EEG) findings with neurodevelopmental outcome.J Child Neurol 2008;23:394–398.

Rowe JC, Holmes GL, Hafford J, et al. Prognostic value of the electroencephalo-gram in term and preterm infants following neonatal seizures. Electroence-phalogr Clin Neurophysiol 1985;60:183–196.

Sainio K, Granstrom ML, Pettay O, Donner M. EEG in neonatal herpes simplexencephalitis. EEG Clin Neurophysiol 1983; 56:556–561.

Scher MS, Beggarly M. Clinical significance of focal periodic discharges in neo-nates. J Child Neurol 1989;4:175–185.

Scher MS, Hamid MY, Steppe DA, et al. Ictal and interictal electrographic seizuredurations in preterm and term neonates. Epilepsia 1993;34:284–288.

Scher MS, Bova JM, Dokianakis SG, Steppe DA. Physiological significance ofsharp wave transients on EEG recordings of healthy pre-term and full-termneonates. Electroencephalogr Clin Neurophysiol 1994;90:179–185.

Scher MS, Bova JM, Dokianakis SG, Steppe DA. Positive temporal sharp waveson EEG recordings of healthy neonates: a benign pattern of dysmaturity inpre-term infants at post-conceptional term ages. Electroencephalogr ClinNeurophysiol 1994;90:173–178.

Scher MS, He BQ, Mazumdar S, et al. A reliability study of a neonatal seizureScoring system. J Epilepsy 1994;7:273–278.

Scher MS, Johnson MW, Holditch-Davis D. Cyclicity of neonatal sleep behaviorsat 25 to 30 weeks’ postconceptional age. Pediatr Res 2005;57:879–882.

Scher MS. Electroencephalography of the newborn: normal and abnormal fea-tures. In: Niedermeyer E, Lopes da Silva FH, eds. Electroencephalography.5th ed. Philadelphia: Lippincott Williams and Wilkins, 2005:937–990.

Shellhaas RA, Clancy RR. Characterization of neonatal seizures by conventionalEEG and single-channel EEG. Clin Neurophysiol 2007;118:2156–2161.

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172 Copyright � 2013 by the American Clinical Neurophysiology Society

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Shellhaas RA, Chang T, Tsuchida T, et al. The American Clinical Neurophysiol-ogy Society’s guideline on continuous electroencephalography monitoring inneonates. J Clin Neurophysiol 2011.

Shewmon DA. What is a neonatal seizure? Problems in definition and quantificationfor investigative and clinical purposes. J Clin Neurophysiol 1990;7:315–368.

Statz A, Dumermuth G, Mieth D, Duc G. Transient EEG patterns during sleep inhealthy newborns. Neuropediatrics 1982;13:115–122.

Tharp BR, Cukier F, Monod N. The prognostic value of the electroencephalo-gram in premature infants. Electroencephalogr Clin Neurophysiol 1981;51:219–236.

Vespa PM, Nenov V, Nuwer MR. Continuous EEG monitoring in the intensivecare unit: early findings and clinical efficacy. J Clin Neurophysiol 1999;16:1–13.

Volpe JJ. Brain death determination in the newborn. Pediatrics 1987;80:293–297.

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